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Mechanisms of Gustatory Coding in Spodoptera Littoralis Alexandra Luminita Popescu

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Mechanisms of Gustatory Coding in Spodoptera Littoralis Alexandra Luminita Popescu Mechanisms of gustatory coding in Spodoptera littoralis Alexandra Luminita Popescu To cite this version: Alexandra Luminita Popescu. Mechanisms of gustatory coding in Spodoptera littoralis. Life Sciences [q-bio]. AgroParisTech, 2008. English. NNT : 2008AGPT0079. pastel-00004445 HAL Id: pastel-00004445 https://pastel.archives-ouvertes.fr/pastel-00004445 Submitted on 20 Mar 2009 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. N° /__/__/__/__/__/__/__/__/__/__/ THÈSE pour obtenir le grade de Docteur de l’Institut des Sciences et Industries du Vivant et de l’Environnement (Agro Paris Tech) présentée et soutenue publiquement par POPESCU Alexandra Le 2 décembre 2008 Mechanisms of gustatory coding in Spodoptera littoralis Directeur de thèse : Frédéric Marion-Poll Codirecteurs de thèse : Sylvia Anton Jean-Pierre Rospars Travail réalisé : INRA, UMR 1272 Physiologie de l’Insecte, Signalisation et Communication, F-78000 Versailles Devant le jury : Prof. Claudio Lazzari; Univ. Tours: Président Prof. Geraldine Wright, Univ. Newcastle, (UK): rapporteur Prof. Joachim Schachtner; Univ. Marburg, (DE): rapporteur Prof. Frédéric Marion-Poll; AgroParisTech: examinateur Dr. Sylvia Anton; INRA: examinateur Dr. Jean-Pierre. Rospars; INRA: examinateur English summary English summary Taste is one of the fundamental senses by which animals can detect food sources (sugars, salts, lipids, amino acids) but also noxious compounds dissolved in aqueous solution or adsorbed on surfaces (leaf, cuticle). Unlike olfaction, where only cephalic organs are involved in the detection of volatile compounds, in insects, gustatory sensilla are located on different parts of the insect body (mouthparts, legs, wings, ovipositor) which results in the precise spatial location of the stimuli which excite them. These sensilla are involved in different behaviours and might therefore be tuned to different types of contact chemosensory stimuli. These functional constraints imply a different organisation of the nervous centres processing the information received from gustatory receptor neurons. Whereas projections from olfactory receptor neurons are clearly chemotopic, comparatively little is known on how gustatory neurons project to the central nervous system and how signals are encoded and processed by central neurons. In different insect species, including Lepidoptera, responses of gustatory receptor neurons situated on the tarsae and the abdomen have been described. However, physiological characteristics of antennal gustatory sensilla and the behavioural context in which they are used are only starting to be investigated. The objectives of this thesis were to study the gustatory neurons of contact chemosensory sensilla present on the antennae of adult Spodoptera littoralis using two different approaches: an electrophysiological approach of testing soluble chemicals and recording the firing pattern of these neurons; and a neuroanatomical approach of staining their pathways and target regions in the brain. Our electrophysiological observations show that taste sensilla possess neurons that respond to sugars like sucrose, fructose and glucose and to NaCl. We could not identify a gustatory receptor neuron responding to bitter compounds or amino acids, but the range of tested substances was limited and nothing is known on the behavioural significance of such compounds. We were able to test the sensitivity along the antenna of the sensilla located on the lateral side of the antenna but no differences were noticed. However, sensilla in males and females differed in sensitivity. In females, the intensity of responses was found to be weaker for the sensilla on the dorsal side of the antennae than for those on the ventral side. Antennation is a behaviour frequently described before mating or egg laying. The precise role of contact chemoreceptors in this kind of behaviours is however, unknown. For a conclusive interpretation of our data on the neuronal coding and central representation of taste English summary information from the antennae, the involvement of antennal gustatory receptors in mating behaviour, host-plant detection and oviposition and their possible interactions with olfactory receptor neurons remains to be investigated. A scanning electron microscopic study showed no sexual dimorphism in the distribution of taste sensilla on the antennae. Mass fills of antennal afferents and backfills of individual contact chemoreceptive sensilla using Neurobiotin revealed 4 distinct projection areas of antennal gustatory sensilla. Two areas are within the deutocerebrum: the antennal motor and mechanosensory centre (AMMC) and a region situated posteriorly to the antennal lobes. The two other areas are in the tritocerebrum/suboesophageal ganglion complex. As our electrophysiological investigations showed that different neurons in the same sensillum respond to different stimuli, including mechanical stimuli for one of the neurons, it can be hypothesized that the projection areas are functionally distinct. No evidence for somatotopy of sensillar afferents originating from different parts of the antenna was found, with the methods used. A more detailed analysis of branching patterns within each target zone might reveal some form of somatotopy, however. 3 Résumé en français Résumé en français La gustation est un sens essentiel à tous les animaux, leur permettant de détecter aussi bien des substances à valeur alimentaire (sucres, sels, lipides, acides aminés) que des substances potentiellement toxiques dissoutes en solution aqueuse ou adsorbées sur des surfaces (feuille, cuticule). Contrairement à l’olfaction qui détecte des substances volatiles diffusées dans l’air ambiant, la gustation est étroitement liée à une localisation spatiale des stimuli, impliquant un positionnement très précis de l’organe sensitif. Ces contraintes fonctionnelles impliquent une structuration complètement différente des centres nerveux traitant les informations issues de ces récepteurs chimiques. Dans le cas de l’olfaction, les projections des récepteurs olfactifs sont clairement chimiotopiques, les afférences olfactives se regroupant sur des zones de convergence en fonction des récepteurs membranaires exprimés dans les neurones olfactifs. Dans le cas de la gustation, les projections des récepteurs gustatifs seraient étroitement associées aux projections des mécanorécepteurs, selon une organisation somatotopique. Par rapport au système olfactif, les connaissances sur le fonctionnement du système nerveux gustatif chez les insectes sont restées en retrait, essentiellement à cause des difficultés inhérentes à la caractérisation des projections et à la difficulté de déterminer si à la somatotopie se superpose une chimiotopie. Nous avons étudie le système gustatif associé aux antennes de lépidoptères, en prenant pour modèle la noctuelle du coton Spodoptera littoralis. Les récepteurs gustatifs des antennes sont impliqués dans différents comportements, comme l’ont montré notamment des protocoles d’apprentissage associatif. Cet organe est remarquable chez les lépidoptères car il est dépourvu de muscles (à l’exception de la base) et caractérisé par la duplication de segments homologues (les segments antennaires) portant une distribution d’organes olfactifs et gustatifs identique de segment à segment, avec néanmoins des différences progressives en allant de la base vers l’extrémité. Nous avons abordé d’abord l’aspect fonctionnel des neurones en caractérisant par des techniques électrophysiologiques le spectre de réponse de ces neurones gustatifs à l’aide de stimuli simples (sucres, sels, acides aminés, composés amers). Dans une deuxième phase du travail, la structuration du système antennaire a été abordée par des marquages cellulaires à la neurobiotine de sensilles gustatives individuelles. Ce travail a été précédé par une cartographie précise de la localisation des sensilles gustatives à la Résumé en français surface de l’antenne, par microscopie électronique à balayage. La caractérisation des projections a nécessité l’utilisation d’outils de reconstruction 3D de manière à pouvoir estimer la constance des projections issues de récepteurs homologues entre différents insectes et à estimer la distribution spatiale des projections issues de neurones différents chez le même insecte. L’antenne de l’espèce S. littoralis est constituée de 3 parties : le scape, le pédicelle et le flagelle. Seul le flagelle, qui est constitué d’environ 70 segments, porte des sensilles gustatives. Chaque segment a une partie ventrale et une partie dorsale. Au niveau de la partie ventrale on trouve 4 sensilles gustatives: 2 latérales et 2 médiales. Les premiers segments situés à la base de l’antenne sont dépourvus de sensilles médiales. On commence à les observer à partir des 6ème-7ème segments à la base de l’antenne. Au niveau du dernier segment situé à l’extrémité, on observe une couronne de sensilles gustatives (6 ou 7). La partie dorsale de l’antenne est couverte d’écailles, mais on peut observer 2 sensilles gustatives médiales au niveau de chaque segment
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